Operational challenges of the Philippine Antimicrobial Resistance Surveillance Program during the COVID-19 pandemic

Problem Operation of the Philippine Antimicrobial Resistance Surveillance Program (ARSP) has been affected by the coronavirus disease 2019 (COVID-19) pandemic, during which time difficulties in maintaining laboratory functions, staffing levels and participation were reported. Context The COVID-19 pandemic has increased pressure on most health systems and programmes in the Philippines, including ARSP. As ARSP is the source of national data on antimicrobial resistance (AMR) trends, there are concerns that the negative effects of the pandemic may have impacted the quality of data produced. Action We describe disruptions to laboratory operations, personnel availability and participation in ARSP surveillance, and their impact on reported data for 2020. Outcome Surveillance operations were challenged by reallocation of human, infrastructure and financial resources for pandemic response among both the sentinel sites and the coordinating laboratory, the Antimicrobial Resistance Surveillance Reference Laboratory. There was a decrease in the amount of data submitted to the surveillance system, as well as in the number of isolates sent to the reference laboratory for confirmation of bacterial identification and antimicrobial susceptibility testing. Nevertheless, overall performance scores of the sentinel sites for most parameters were comparable to 2019, the year before the pandemic. Discussion The impact of operational changes to ARSP due to the pandemic needs to be considered when analysing AMR surveillance data from 2020. Automation of data submission, good working relationships between the coordinating laboratory and sentinel sites, and supply chain system strengthening were identified as key to maintaining AMR surveillance during the COVID-19 pandemic.

for 2019 ( Table 1). The set of indicators and targets had been jointly agreed upon by the sentinel sites and ARSRL during previous annual meetings. Information about how the COVID-19 pandemic had affected sentinel site participation in ARSP was gathered from the site status reports that were presented at the ARSP PIM, in particular, the responses to the following questions that sites had been asked to provide: 1) How has the COVID-19 pandemic affected your laboratory operations? and 2) How has the COVID-19 pandemic affected your participation in ARSP?

Laboratory operations
All 26 sentinel sites reported experiencing operational challenges, which varied in type and extent. Most (18/26, 69.2%) of the sentinel sites cited delays in the usual schedule of delivery of reagents and supplies due to transportation issues. Another commonly reported supply challenge stemmed from the new requirement to use extra layers of PPE, which resulted in episodes of low or depleted supplies of PPE at nearly two thirds (17/26, 65.4%) of sites. In some areas, suspension of courier services had reportedly delayed the referral of bacterial isolates to RITM for confirmatory testing.
Half (13/26, 50%) of all sentinel sites reported a decrease in the number of specimens requiring routine culture and sensitivity testing. Four reported periodic closure of their outpatient departments. Sites also reported a low influx of patients, and the two nongovernment sentinel sites experienced a reduction in revenue for the laboratory.

Laboratory personnel
The majority (14/26, 53.9%) of sentinel sites reported being designated as COVID-19 referral hospitals during the pandemic and having to establish or expand their molecular biology facilities. Even though this provided opportunities for acquisition of new equipment and increasing laboratory staff capacity for molecular detection of pathogens, it also meant temporary reallocation of space and human resources for RT-PCR testing for COVID-19.
The majority of sentinel sites also reported encountering various challenges relating to laboratory personnel.
RITM has been at the forefront of the Philippine COVID-19 response for both patient care and laboratory testing. From January to June 2020, RITM served as the primary COVID-19 testing centre for the Philippines, responsible for more than 90% of all COVID-19 tests conducted in the country. In March 2020, to accommodate the surge in demand for reverse transcription polymerase chain reaction (RT-PCR) testing for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), ARSRL, together with RITM's other laboratories, was directed to assist the national testing effort by undertaking some of the procedures required, such as sample inactivation and DNA extraction. This directive resulted in the reassignment of ARSRL laboratory staff to the COVID-19 testing team. Facilities, workspaces, equipment and critical resources (reagents, supplies, consumables and personal protective equipment [PPE]) were also repurposed to meet the demand for COVID-19 testing. Directives were also made to postpone scheduled trainings, monitoring visits and face-to-face meetings -activities usually performed by the reference laboratory -until the end of June 2020. Consequently, the number of laboratory technicians who underwent training for AMR bacteriology procedures decreased from 27 to 6.
By July 2020, sufficient additional staff had been recruited to cover the COVID-19 response tasks, allowing existing reference laboratory staff to return to their routine AMR surveillance work. However, until the end of 2020 about 20% of ARSRL laboratory space remained allocated to the COVID-19 response. The annual ARSP Program Implementation Meeting (ARSP PIM) was held virtually via Zoom instead of the usual face-to-face format and the publication of the ARSP 2019 annual surveillance report was delayed by 5 months.

ACTION
The impacts of the above-mentioned institutional directives on the operations of RITM's ARSRL were reviewed. In addition, the challenges experienced by the surveillance sentinel sites participating in ARSP during the course of 2020 were summarized.
In order to assess the impact of the pandemic, ARSP performance indicators (and corresponding targets for participation and number of isolates reported to the surveillance system) for 2020 were compared to those to be at work. Laboratory personnel from four sites in the National Capital Region (NCR) reported experiencing difficulties in getting to work due to travel restrictions and suspension of transport services.

Participation in ARSP
Delays in transporting isolates to ARSRL for confirmatory testing, typically because of the lack of courier services, was a common challenge among sentinel sites (9/26, 34.6%). Moreover, the decrease in the number of samples requiring testing at sentinel sites also reduced the demand for confirmatory testing of isolates.
Although automated transmission of data from the sentinel sites to ARSRL had already been established Seventeen sites (65.4%) experienced a reduction in the number of active-duty staff over several periods due to reassignment to other hospital units for COVID-19 sample processing and testing. Furthermore, around one third (9/26, 34.6%) reported that on several occasions staff work schedules had to be reduced to a skeletal workforce to maintain physical distancing in the laboratory. Staff in high-risk groups were ordered to work from home, further decreasing the number of staff available to work in bacteriology laboratories. Eleven sentinel sites (42.3%) reported that they were provided with additional manpower to help overcome staffing challenges.
The health status of frontline workers at ARSP sites was also affected, with some infected with COVID-19 and some experiencing anxiety because of the requirement

Comparison of ARSP data submission: 2019 versus 2020
Across all sentinel sites, the number of AST data submissions dropped by 38.7%, from a total of 100 334 in 2019 to 61 527 in 2020 ( Table 2). All sentinel sites in the NCR recorded substantial decreases in reported data, with two sentinel sites unable to submit any AST data at all in 2020. Relative to the NCR, sites in Visayas had smaller decreases in test data submissions, with one site reporting a 5% increase. In Mindanao, a decrease was observed in four out of the six sites ( Table 2).

Lessons learnt
Sentinel sites that submitted the same or increased volumes of AMR surveillance data in 2020 were asked to explain how they were able to maintain their 2019 levels of performance despite the pandemic. At Site 26, a gonococcal surveillance site, scheduled testing for sex workers continued despite the pandemic, resulting in an increase in submissions, a commendable achievement and one that highlights the importance of retaining AMR surveillance for gonococcal infections. Site 20's increase in submitted data may have been due to the increase in the number of admissions due to COVID-19 infections, which prompted an increase in requests for AST, especially for those admitted for respiratory symptoms. Site 24 reported that they were able to mitigate challenges related to procurement of laboratory reagents and supplies by strengthening communications and coordination with suppliers regarding possible delays, changes and expiration dates of goods for delivery.
prior to the pandemic, many sentinel sites still reported experiencing delays in encoding identification and susceptibility data to WHONET due to decreased staff numbers in their bacteriology sections. There was, however, a reduction in the amount of surveillance data submitted in 2020, a factor that must be considered when interpreting the overall AMR rates reported by ARSP for 2020. It is possible that the decrease in submitted data was due to the shift towards remote outpatient consultations (to lessen the risk of infection at the sentinel sites), a trend which could introduce bias in patient and testing denominators for the 2020 ARSP surveillance data, and which should be considered in the analysis of AMR data. 6,7 The actions implemented by the participating sentinel sites alleviated much of the negative impact of the pandemic on laboratory operations and logistics. Performance indicators revealed that despite the ongoing health crisis, sentinel sites were able to perform their tasks as the primary contributors to national AMR data collection. It is imperative for ARSRL to disseminate information and encourage other facilities to adopt the good practices observed at these sites. The success and continuity of ARSP is contingent upon the collaborative efforts of the reference laboratory and the sentinel sites. The COVID-19 pandemic has the potential to exacerbate the AMR situation in the Philippines and put stewardship efforts at risk. It is imperative therefore that efforts against the development of AMR should not cease.
Further studies should be conducted to provide more information on the impact of the COVID-19 pandemic on AMR emergence and spread. Moreover, the expanded molecular biology facilities established to meet the needs of the COVID-19 response should be utilized to enhance national AMR surveillance through genomic epidemiology.
Practices that proved useful in overcoming challenges caused by the COVID-19 pandemic included prompt preparation of a procurement plan for reagents and supplies for COVID-19 testing, which helped minimize the risk of depletion of supplies; establishment of a process for sharing laboratory supplies among the reference laboratory and sentinel sites; and use of logistics created for the COVID-19 pandemic to support AMR surveillance (i.e. some sentinel sites were able to send both isolates for AST and samples for COVID-19 testing to RITM simultaneously).

DISCUSSION
The challenges to ARSP laboratory operations, including staffing, experienced during the COVID-19 pandemic did not appear to reduce overall participation of the sentinel sites in ARSP. This could be due, at least in part, to the fact that all sentinel sites, having been involved in ARSP for more than 5 years, have surveillance activities ingrained in their operations such that the disruptions of the COVID-19 pandemic did not result in lessened participation in surveillance activities. However, we recognize the limitation that the activity reports provided by each site may not have included other relevant aspects of laboratory operations. Estimated changes in the performance indicators reported here cannot therefore be conclusively attributed to the actions described by the sentinel sites in their activity reports.
The good working relationships between RITM and sentinel site personnel, formed through partnerships that have been in place since 1988, may have been a contributory factor in maintaining high levels of participation in ARSP. The practice of recognizing and incentivizing sites with top participation scores, which was established in 2012, may have also encouraged continued participation in ARSP during the COVID-19 pandemic.
The process of automated data transfer, whereby WHONET encoded data from the sentinel sites are automatically transmitted to the ARSRL server, facilitated the data submission from sentinel sites throughout 2020. ARSRL, as the coordinating laboratory, adapted to the challenges caused by the pandemic by adjusting staff schedules and activities, holding the annual PIM